Genetic relatedness in groups of the humbug damselfish Dascyllus aruanus: small, similar-sized individuals may be close kin

Kin selection plays an important role in the evolution of social behaviour in terrestrial systems. The extent to which kin selection influences the evolution of social behaviour in marine systems is largely unexplored. Generally, it is considered that kin selection is irrelevant in marine systems, because it is assumed that the dispersing larval phase of marine organisms will break up kin associations. Here, we challenge this assumption and investigate the opportunity for kin selection in a coral reef fish: the humbug damselfish Dascyllus aruanus . This fish lives in groups composed of a large male and a number of smaller females and nonbreeders. We use 10 polymorphic microsatellite loci to assess the relatedness of 265 individuals from 35 groups. The mean coefficient of relatedness among group members is 0.01 ± 0.04, suggesting that individuals are not associated with close relatives. However, the distribution of pairwise relatedness of individuals within groups has an overabundance of positive values, and indicates that there might be 35 pairs of close relatives within groups. Further analyses reveal that close relatives likely are similar in size and small in size, suggesting that they might have recruited together. We conclude that it is possible for kin selection to operate in D. aruanus , but kin recognition will be a prerequisite for such selection. This study reveals that individuals can be associated with close relatives, and there is a hidden potential for kin selection, during certain parts of the life cycle of coral reef fishes.     

Advanced eusociality, kin selection and male haploidy

Abstract  The generation-long primacy of kin selection in explaining the evolution of advanced eusociality in social insects has been challenged in recent papers. Does this challenge succeed? I consider three questions: is kin selection still the unchallengeable explanation for the evolution of eusociality; is the male haploidy of Hymenoptera important in this explanation; and, a subsidiary question of why are there no male workers in Hymenoptera? I briefly trace the origins of kin selection back to Darwin and then consider the explanations of mutualism, group selection, parental manipulation, and kin selection and its variant 'green beard' alleles. I stress that in the kin selection equation, however written, relatedness is deeply intertwined with ecology so that both are essential. Kin selection does remain unchallengeable but, for some, the role of male haploidy has lost favour recently despite several modelling efforts all finding that it favours the evolution of eusociality. Sex allocation is deep at the heart of the evolution of hymenopteran advanced eusociality, indicating the interacting roles of population genetics and general biology. Modellers have also found no reason for a lack of male workers, so that a biological superiority of females for this role is indicated for social Hymenoptera.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco (Ctenomys talarum), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.     

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.     

The evolution of alternative cryptic female choice strategies in age-structured populations

Abstract.— Cryptic female choice is a potentially important aspect of the sexual selection process. According to the theory of sexual dialectics, postcopulation manipulation of relative male fertilization success can provide an avenue by which females can circumvent attempts by males to control female reproduction. Here I use stochastic models to investigate the evolution of cryptic female choice in populations with and without age structure. In populations without age structure, cryptic female choice will evolve only when (1) precopulatory mate choice by females is inefficient, (2) variation in male fitness is correlated with a trait upon which a female can base her choice of mates, and (3) the cost of multiple mating is not too high. In populations with age structure, similar conditions apply. However, selection sometimes favors females that employ alternative strategies of female choice at different ages. These results help to define the types of biological systems in which we should expect to see the evolution of cryptic female choice. They also illustrate that the evolution of choice strategies in females may be complex and may mirror in some important respects the evolution of alternative mating tactics in males.     

Male Androphilia in the Ancestral Environment

The kin selection hypothesis posits that male androphilia (male sexual attraction to adult males) evolved because androphilic males invest more in kin, thereby enhancing inclusive fitness. Increased kin-directed altruism has been repeatedly documented among a population of transgendered androphilic males, but never among androphilic males in other cultures who adopt gender identities as men. Thus, the kin selection hypothesis may be viable if male androphilia was expressed in the transgendered form in the ancestral past. Using the Standard Cross-Cultural Sample (SCCS), we examined 46 societies in which male androphilia was expressed in the transgendered form (transgendered societies) and 146 comparison societies (non-transgendered societies). We analyzed SCCS variables pertaining to ancestral sociocultural conditions, access to kin, and societal reactions to homosexuality. Our results show that ancestral sociocultural conditions and bilateral and double descent systems were more common in transgendered than in non-transgendered societies. Across the entire sample, descent systems and residence patterns that would presumably facilitate increased access to kin were associated with the presence of ancestral sociocultural conditions. Among transgendered societies, negative societal attitudes toward homosexuality were unlikely. We conclude that the ancestral human sociocultural environment was likely conducive to the expression of the transgendered form of male androphilia. Descent systems, residence patterns, and societal reactions to homosexuality likely facilitated investments in kin by transgendered males. Given that contemporary transgendered male androphiles appear to exhibit elevated kin-directed altruism, these findings further indicate the viability of the kin selection hypothesis.     

Patterns of coalition formation by adult female baboons in Amboseli, Kenya

Coalitionary support in agonistic interactions is generally thought to be costly to the actor and beneficial to the recipient. Explanations for such cooperative interactions usually invoke kin selection, reciprocal altruism or mutualism. We evaluated the role of these factors and individual benefits in shaping the pattern of coalitionary activity among adult female savannah baboons, Papio cynocephalus, in Amboseli, Kenya. There is a broad consensus that, when ecological conditions favour collective defence of resources, selection favours investment in social relationships with those likely to provide coalitionary support. The primary features of social organization in female-bonded groups, including female philopatry, linear dominance hierarchies, acquisition of maternal rank and well-differentiated female relationships, are thought to be functionally linked to the existence of alliances between females. Female savannah baboons display these characteristics, but the frequency and function of their coalitionary aggression is disputed. In our five study groups, 4-6% of all disputes between females led to intervention by third parties. Adult females selectively supported close maternal kin. There was no evidence that females traded grooming for support or reciprocated support with nonkin. High-ranking females participated in coalitionary aggression most frequently, perhaps because they derived more benefits from group membership than other females did or could provide support at lower cost. Females typically supported the higher ranking of two contestants when they intervened in disputes between subordinates, so most coalitions reinforced the existing dominance hierarchy. Results indicate that female baboons participate in coalitionary aggression in a manner strongly influenced by nepotism and individual benefits.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.     

Family feuds: social competition and sexual conflict in complex societies

Darwin was initially puzzled by the processes that led to ornamentation in males-what he termed sexual selection-and those that led to extreme cooperation and altruism in complex animal societies-what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities-particularly in females-and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.     

Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites

Complex eusocial insect societies are generally matrifilial, suggesting kin selection has been of importance in their development. For simpler social systems, factors favouring their existence, in particular kin selection, have rarely been studied. Communal nesting is one of these simple social organizations, and is found in a diversity of insect species. To examine whether kin selection may play a role in the evolution and maintenance of communality, we estimated genetic relatedness of nestmate females of the facultatively communal bee, Andrena jacobi . Microsatellite loci were developed for this species and used to analyse individuals from two populations. Loci were variable, they were in heterozygote deficit and showed positive inbreeding coefficients. This may arise from nonrandom mating; previous observations (Paxton & Tengö 1996) indicate that a large proportion of females mate intranidally with nestmate males in their natal nests before first emerging. Nestmate relatedness was low, no different from zero for all loci in one population and for three of four loci in the other population. The large number of nestmates sharing a common nest (up to 594) may explain the low relatedness estimates, although relatedness was also independent of the number of females sharing a nest. Lack of inclusive fitness payoffs could constrain social evolution in this communal species.     

Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher, Ramphocinclus brachyurus

Dispersal is a fundamental process influencing evolution, social behaviour, and the long-term persistence of populations. We use both observational and genetic data to investigate dispersal, kin-clustering and intergroup relatedness in the white-breasted thrasher, Ramphocinclus brachyurus, a cooperatively breeding bird that is globally endangered. Mark-resighting data suggested sex-biased dispersal, with females dispersing over greater distances while males remained philopatric. Accordingly, spatial autocorrelation analysis showed highly significant fine-scale genetic structure among males, but not among females. This fine-scale genetic structuring of the male population resulted in very high levels of relatedness between dominant males at neighbouring nests, similar to that seen within cooperative groups in many species where kin selection is cited as a cause of cooperation. By implication, between-group as well as within-group cooperation may be important, potentially creating a feedback loop in which short-distance dispersal by males leads to the formation of male kin clusters that in turn facilitate nepotistic interactions and favour further local recruitment. The strength of spatial autocorrelation, as measured by the autocorrelation coefficient, r, was approximately two to three times greater than that reported in previous studies of animals. Relatively short dispersal distances by both males and females may have a negative impact on the white-breasted thrasher's ability to colonize new areas, and may influence the long-term persistence of isolated populations. This should be taken into account when designating protected areas or selecting sites for habitat restoration.     

Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus

The brown long-eared bat, Plecotus auritus, is unusual among temperate zone bats in that summer maternity colonies are composed of adult males and females, with both sexes displaying natal philopatry and long-term association with a colony. Here, we describe the use of microsatellite analysis to investigate colony relatedness and mating patterns, with the aim of identifying the evolutionary determinants of social organization in P. auritus. Mean colony relatedness was found to be low (R=0.033 +/- 0.002), with pairwise estimates of R within colonies ranging from -0.4 to 0.9. The proportion of young fathered by males in their own colony was investigated using a Bayesian approach, incorporating parameters detailing the number of untyped individuals. This analysis revealed that most offspring were fathered by males originating from a different colony to their own. In addition, we determined that the number of paternal half-sibs among cohorts of young was low, inferring little or no skew in male reproductive success. The results of this study suggest that kin selection cannot account for colony stability and natal philopatry in P. auritus, which may instead be explained by advantages accrued through the use of familiar and successful roost sites, and through long-term associations with conspecifics. Moreover, because the underlying causes of male natal dispersal in mammals, such as risk of inbreeding or competition for mates, appear to be avoided via extra-colony copulation and low male reproductive skew, both P. auritus males and females are able to benefit from long-term association with the natal colony.     

Male reproductive skew, paternal relatedness, and female social relationships

Female social relationships among primates are thought to be shaped by socio-ecological factors and phylogenetic constraints. We suggest that patterns of paternal relatedness among females influence measures of social tolerance that have been used to classify species into different social relationship categories. As kin support and kin preference have only been measured for matrilineal kin and related individuals exchange less aggression and have a higher conciliatory tendency, the observed low nepotism levels and high tolerance levels may be an artifact of hidden paternal relatedness among the nonkin category. Using comparative data on macaques, we investigate this hypothesis using male reproductive skew as a proxy for paternal relatedness. Within the limitations of the study we show that populations classified as being less nepotistic, and more tolerant exhibit higher levels of reproductive skew. This first result and the reasoning behind may motivate future students of social relationships to take paternal relatedness into consideration. Potential implications of this finding if repeated with larger samples include that variation in aspects of macaque social relationships may be explained without considering phylogeny or the strength of between-group contest competition for food.     

Evolution of sex ratios in social hymenoptera: kin selection,local mate competition,polyandry and kin recognition

A model is constructed to study the effects of local mate competition and multiple mating on the optimum allocation of resources between the male and female reproductive brood in social hymenopteran colonies from the ‘points of view’ of the queen (parental manipulation theory) as well as the workers (kin selection theory). Competition between pairs of alleles specifying different sex investment ratios is investigated in a game theoretic frame work. All other things being equal, local mate competition shifts the sex allocation ratio in favour of females both under queen and worker control. While multiple mating has no effect on the queen’s optimum investment ratio, it leads to a relatively male biased investment ratio under worker control. Under queen control a true Evolutionarily Stable Strategy(ess) does not exist but the ‘best’ strategy is merely immune from extinction. A trueess exists under worker control in colonies with singly mated queens but there is an asymmetry between the dominant and recessive alleles so that for some values of sex ratio a recessive allele goes to fixation but a dominant allele with the same properties fails to do so. Under multiple mating, again, a trueess does not exist but a frequency dependent region emerges. The best strategy here is one that is guaranteed fixation against any competing allele with a lower relative frequency. Our results emphasize the need to determine levels of local mate competition and multiple mating before drawing any conclusions regarding the outcome of queen-worker conflict in social hymenoptera. Multiple mating followed by sperm mixing, both of which are known to occur in social hymenoptera, lower average genetic relatedness between workers and their reproductive sisters. This not only shifts the optimum sex ratio from the workers’ ‘point of view’ in favour of males but also poses problems for the kin selection theory. We show that kin recognition resulting in the ability to invest in full but not in half sisters reverts the sex ratio back to that in the case of single mating and thus completely overcomes the hurdles for the operation of kin selection.     

雌性黄山短尾猴回避近亲交配

本研究分别在交配期(2006年9月-2006年12月)和产仔期(2007年1月-2007年4月)对黄山短尾猴鱼鳞坑YA1群中5只雄猴和5只雌猴成年个体采用目标动物法、随机取样法和连续记录法记录行为参数。研究期间记录交配行为336例:母子交配0例;母系兄妹交配7例(占2.1%),其中强行交配4例;非亲缘关系交配329例(占97.9%),非亲缘关系交配频次显著高于亲缘关系。在交配期,雄猴对亲缘雌猴跟随、性检查频次均低于非亲缘雌猴,接近指数(PMI)在亲缘和非亲缘雌猴间无显著性差异;雌猴对亲缘雄猴交配拒绝率显著高于非亲缘雄猴,接近指数在交配期显著低于非亲缘雄猴,产仔期接近指数在亲缘和非亲缘雄猴间无显著性差异。尽管雄猴在交配选择上趋于避免与亲缘雌猴交配,但某些雄猴仍会主动对有亲缘关系的雌猴邀配或强行交配,雌猴则主动回避。这些结果表明:黄山短尾猴母系亲属间可以通过行为倾向抑制近亲交配发生,且雌猴更主动回避交配,支持了近交回避的双亲投资理论。     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

Kin‐bias,breeding site selection and female fitness in a cannibalistic Neotropical frog

Resource availability influences sexual selection within populations and determines whether behaviours such as territoriality or resource sharing are adaptive. In Thoropa taophora, a frog endemic to the Atlantic Coastal Rainforest of Brazil, males compete for and defend limited breeding sites while females often share breeding sites with other females; however, sharing breeding sites may involve costs due to cannibalism by conspecific tadpoles. We studied a breeding population of T. taophora to determine (i) whether this species exhibits polygynous mating involving female choice for territorial males and limited breeding resources; (ii) whether limited breeding resources create the potential for male–male cooperation in defence of neighbouring territories; and (iii) whether females sharing breeding sites exhibit kin‐biased breeding site choice, possibly driven by fitness losses due to cannibalism among offspring of females sharing sites. We used microsatellites to reconstruct parentage and quantify relatedness at eight breeding sites in our focal population, where these sites are scarce, and in a second population, where sites are abundant. We found that at localities where the appropriate sites for reproduction are spatially limited, the mating system for this species is polygynous, with typically two females sharing a breeding site with a male. We also found that females exhibit negative kin‐bias in their choice of breeding sites, potentially to maximize their inclusive fitness by avoiding tadpole cannibalism of highly related kin. Our results indicate that male territorial defence and female site sharing are likely important components of this mating system, and we propose that kinship‐dependent avoidance in mating strategies may be more general than previously realized.     

Females avoid manipulative males and live longer

Abstract Female mate choice has been demonstrated in a wide variety of species and is now accepted as an important factor in sexual selection. One of the remaining questions, however, is why females prefer specific males. Do females or their offspring benefit from their choice? Or do females choose mates to minimize costs of mating? Here we show that, in the ovoviviparous cockroach Nauphoeta cinerea, where sexual selection has been well documented, females chose mates to avoid costly male manipulation. Females were partnered with preferred or nonpreferred mates, and fitness of the females measured. We found that females lived longer when they mated with preferred males. Female lifespan depended on the rate at which offspring developed from egg to parturition: slower development led to longer life. We manipulated the male pheromone and showed that the component of the pheromone blend that makes males attractive to females also delayed parturition. Thus, like other aspects of sexual conflict in this species, offspring development and thereby the mother's lifespan depended on exposure of females to specific components of the male pheromone. Males benefit from manipulating offspring development because females with accelerated parturition remained unreceptive whereas females with slower developing offspring readily remated after giving birth to their offspring. Our results suggest a hormone‐like role for the male pheromone in N. cinerea and provide the first direct evidence of mate choice to avoid male manipulation. This study shows that dominant males may not be preferred males if they are manipulating females, why multiple components with contrasting effects can exist in a sexual signal, and emphasizes the complex fitness relationships that can arise in species with sexual conflict.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.